{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,15]],"date-time":"2026-09-15T10:44:44Z","timestamp":1789469084586,"version":"build-2803163510"},"reference-count":183,"publisher":"MDPI AG","issue":"23","license":[{"start":{"date-parts":[[2021,11,30]],"date-time":"2021-11-30T00:00:00Z","timestamp":1638230400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000057","name":"National Institute of General Medical Sciences","doi-asserted-by":"publisher","award":["R01GM112715"],"award-info":[{"award-number":["R01GM112715"]}],"id":[{"id":"10.13039\/100000057","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000065","name":"National Institute of Neurological Disorders and Stroke","doi-asserted-by":"publisher","award":["R01NS107383"],"award-info":[{"award-number":["R01NS107383"]}],"id":[{"id":"10.13039\/100000065","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Human and animal studies have elucidated the apparent neurodevelopmental effects resulting from neonatal anesthesia. Observations of learning and behavioral deficits in children, who were exposed to anesthesia early in development, have instigated a flurry of studies that have predominantly utilized animal models to further interrogate the mechanisms of neonatal anesthesia-induced neurotoxicity. Specifically, while neonatal anesthesia has demonstrated its propensity to affect multiple cell types in the brain, it has shown to have a particularly detrimental effect on the gamma aminobutyric acid (GABA)ergic system, which contributes to the observed learning and behavioral deficits. The damage to GABAergic neurons, resulting from neonatal anesthesia, seems to involve structure-specific changes in excitatory-inhibitory balance and neurovascular coupling, which manifest following a significant interval after neonatal anesthesia exposure. Thus, to better understand how neonatal anesthesia affects the GABAergic system, we first review the early development of the GABAergic system in various structures that have been the focus of neonatal anesthesia research. This is followed by an explanation that, due to the prolonged developmental curve of the GABAergic system, the entirety of the negative effects of neonatal anesthesia on learning and behavior in children are not immediately evident, but instead take a substantial amount of time (years) to fully develop. In order to address these concerns going forward, we subsequently offer a variety of in vivo methods which can be used to record these delayed effects.<\/jats:p>","DOI":"10.3390\/ijms222312951","type":"journal-article","created":{"date-parts":[[2021,11,30]],"date-time":"2021-11-30T23:22:28Z","timestamp":1638314548000},"page":"12951","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":23,"title":["Early Development of the GABAergic System and the Associated Risks of Neonatal Anesthesia"],"prefix":"10.3390","volume":"22","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-2667-3225","authenticated-orcid":false,"given":"David A.","family":"Gascoigne","sequence":"first","affiliation":[{"name":"Department of Radiology, NorthShore University HealthSystem, Evanston, IL 60201, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Natalya A.","family":"Serdyukova","sequence":"additional","affiliation":[{"name":"Department of Biomedical Engineering, Northwestern University, Evanston, IL 60208, USA"},{"name":"Department of Pediatrics, NorthShore University HealthSystem, Evanston, IL 60201, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4599-0290","authenticated-orcid":false,"given":"Daniil P.","family":"Aksenov","sequence":"additional","affiliation":[{"name":"Department of Radiology, NorthShore University HealthSystem, Evanston, IL 60201, USA"},{"name":"Department of Anesthesiology, NorthShore University HealthSystem, Evanston, IL 60201, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,11,30]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"513","DOI":"10.1111\/pan.13359","article-title":"Epidemiology of general anesthesia prior to age 3 in a population-based birth cohort","volume":"28","author":"Shi","year":"2018","journal-title":"Paediatr. Anaesth."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"796","DOI":"10.1097\/01.anes.0000344728.34332.5d","article-title":"Early exposure to anesthesia and learning disabilities in a population-based birth cohort","volume":"110","author":"Wilder","year":"2009","journal-title":"Anesth."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"551","DOI":"10.1016\/j.jclinane.2014.03.013","article-title":"Effect of one anesthetic exposure on long-term behavioral changes in children","volume":"26","author":"Chemaly","year":"2014","journal-title":"J. Clin. Anesth."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1270","DOI":"10.1213\/ANE.0b013e3182a9667f","article-title":"General anesthesia in infancy is associated with learning disabilities-or not","volume":"117","author":"Crosby","year":"2013","journal-title":"Anesth. Analg."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"i61","DOI":"10.1093\/bja\/aeq302","article-title":"Early childhood general anaesthesia exposure and neurocognitive development","volume":"105","author":"Sun","year":"2010","journal-title":"Br. J. Anaesth."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1016\/j.expneurol.2015.03.028","article-title":"Neurodevelopmental implications of the general anesthesia in neonate and infants","volume":"272","author":"Lee","year":"2015","journal-title":"Exp. Neurol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"535","DOI":"10.1097\/01.aco.0000433061.59939.b7","article-title":"Anesthetic neurotoxicity in the newborn and infant","volume":"26","author":"Olsen","year":"2013","journal-title":"Curr. Opin. Anaesthesiol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1419","DOI":"10.1213\/ANE.0b013e318299a7c2","article-title":"The effects of exposure to general anesthesia in infancy on academic performance at age 12","volume":"117","author":"Bong","year":"2013","journal-title":"Anesth. Analg."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"2779","DOI":"10.1038\/s41598-019-39174-6","article-title":"Repeated neonatal isoflurane exposures in the mouse induce apoptotic degenerative changes in the brain and relatively mild long-term behavioral deficits","volume":"9","author":"Maloney","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"i29","DOI":"10.1093\/bja\/aet173","article-title":"Propofol-induced apoptosis of neurones and oligodendrocytes in fetal and neonatal rhesus macaque brain","volume":"110","author":"Creeley","year":"2013","journal-title":"Br. J. Anaesth."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"979","DOI":"10.1097\/ALN.0b013e318234228b","article-title":"Neonatal desflurane exposure induces more robust neuroapoptosis than do isoflurane and sevoflurane and impairs working memory","volume":"115","author":"Kodama","year":"2011","journal-title":"J. Am. Soc. Anesthesiol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"524","DOI":"10.1093\/bja\/aex123","article-title":"Isoflurane exposure for three hours triggers apoptotic cell death in neonatal macaque brain","volume":"119","author":"Noguchi","year":"2017","journal-title":"Br. J. Anaesth."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"628","DOI":"10.1097\/ALN.0b013e3181974fa2","article-title":"Neonatal exposure to sevoflurane induces abnormal social behaviors and deficits in fear conditioning in mice","volume":"110","author":"Satomoto","year":"2009","journal-title":"J. Am. Soc. Anesthesiol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"834","DOI":"10.1097\/ALN.0b013e3181d049cd","article-title":"Isoflurane-induced neuroapoptosis in the neonatal rhesus macaque brain","volume":"112","author":"Brambrink","year":"2010","journal-title":"J. Am. Soc. Anesthesiol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"559","DOI":"10.1002\/dev.21963","article-title":"Impact of anesthesia exposure in early development on learning and sensory functions","volume":"62","author":"Aksenov","year":"2020","journal-title":"Dev. Psychobiol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1097\/ALN.0000000000000477","article-title":"Long-term effects of single or multiple neonatal sevoflurane exposures on rat hippocampal ultrastructure","volume":"122","author":"Amrock","year":"2015","journal-title":"Anesthesiology"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"664","DOI":"10.1016\/S0140-6736(18)32485-1","article-title":"Neurodevelopmental outcome at 5 years of age after general anaesthesia or awake-regional anaesthesia in infancy (GAS): An international, multicentre, randomised, controlled equivalence trial","volume":"393","author":"McCann","year":"2019","journal-title":"Lancet"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1016\/S0140-6736(15)00608-X","article-title":"Neurodevelopmental outcome at 2 years of age after general anaesthesia and awake-regional anaesthesia in infancy (GAS): An international multicentre, randomised controlled trial","volume":"387","author":"Davidson","year":"2016","journal-title":"Lancet"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"2312","DOI":"10.1001\/jama.2016.6967","article-title":"Association Between a Single General Anesthesia Exposure Before Age 36 Months and Neurocognitive Outcomes in Later Childhood","volume":"315","author":"Sun","year":"2016","journal-title":"JAMA"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1097\/ALN.0000000000002232","article-title":"Neuropsychological and Behavioral Outcomes after Exposure of Young Children to Procedures Requiring General Anesthesia: The Mayo Anesthesia Safety in Kids (MASK) Study","volume":"129","author":"Warner","year":"2018","journal-title":"Anesthesiology"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"851","DOI":"10.1016\/j.jpedsurg.2021.01.002","article-title":"The effects of early anesthesia on neurodevelopment: A systematic review","volume":"56","author":"Grabowski","year":"2021","journal-title":"J. Pediatr. Surg."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Feng, Y.P., Yang, T.S., Chung, C.H., Chien, W.C., and Wong, C.S. (2020). Early childhood general anesthesia exposure associated with later developmental delay: A national population-based cohort study. PLoS ONE, 15.","DOI":"10.1371\/journal.pone.0238289"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"368","DOI":"10.1016\/j.neuropharm.2018.03.030","article-title":"Brain tissue oxygen regulation in awake and anesthetized neonates","volume":"135","author":"Aksenov","year":"2018","journal-title":"Neuropharmacology"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"153","DOI":"10.2147\/DDDT.S163197","article-title":"Neuroprotective effects of dexmedetomidine against isoflurane-induced neuronal injury via glutamate regulation in neonatal rats","volume":"13","author":"Wang","year":"2019","journal-title":"Drug Des. Dev. Ther."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"26","DOI":"10.3389\/fnsys.2020.00026","article-title":"Neonatal Ketamine Alters High-Frequency Oscillations and Synaptic Plasticity in the Subiculum But Does not Affect Sleep Macrostructure in Adolescent Rats","volume":"14","author":"Manzella","year":"2020","journal-title":"Front. Syst. Neurosci."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"845","DOI":"10.1213\/ANE.0b013e318281e988","article-title":"Characterization and quantification of isoflurane-induced developmental apoptotic cell death in mouse cerebral cortex","volume":"116","author":"Istaphanous","year":"2013","journal-title":"Anesth. Analg."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1016\/S0079-6123(06)60005-8","article-title":"The cellular, molecular and ionic basis of GABA(A) receptor signalling","volume":"160","author":"Farrant","year":"2007","journal-title":"Prog Brain Res"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"260","DOI":"10.1016\/j.neuron.2016.06.033","article-title":"GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits","volume":"91","author":"Tremblay","year":"2016","journal-title":"Neuron"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"10082","DOI":"10.1523\/JNEUROSCI.19-22-10082.1999","article-title":"Total number and ratio of excitatory and inhibitory synapses converging onto single interneurons of different types in the CA1 area of the rat hippocampus","volume":"19","author":"Gulyas","year":"1999","journal-title":"J. Neurosci."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"527","DOI":"10.1016\/S0306-4522(00)00496-6","article-title":"Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells","volume":"102","author":"Megias","year":"2001","journal-title":"Neuroscience"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1016","DOI":"10.1016\/j.neuron.2016.01.029","article-title":"Structured Dendritic Inhibition Supports Branch-Selective Integration in CA1 Pyramidal Cells","volume":"89","author":"Bloss","year":"2016","journal-title":"Neuron"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"664706","DOI":"10.3389\/fneur.2021.664706","article-title":"Normal Development of Local Neurovascular Interactions and the Diagnostic Value of Resting State Functional MRI in Neurovascular Deficiency Based on the Example of Neonatal Anesthesia Exposure","volume":"12","author":"Aksenov","year":"2021","journal-title":"Front. Neurol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"232","DOI":"10.1038\/nature09613","article-title":"Glial and neuronal control of brain blood flow","volume":"468","author":"Attwell","year":"2010","journal-title":"Nature"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1177\/1073858417703033","article-title":"Mechanisms Mediating Functional Hyperemia in the Brain","volume":"24","author":"Nippert","year":"2018","journal-title":"Neuroscientist"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1038\/nrn3168","article-title":"Understanding calcium waves and sparks in central neurons","volume":"13","author":"Ross","year":"2012","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"7583","DOI":"10.1073\/pnas.91.16.7583","article-title":"Nitric oxide and cGMP cause vasorelaxation by activation of a charybdotoxin-sensitive K channel by cGMP-dependent protein kinase","volume":"91","author":"Archer","year":"1994","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"416","DOI":"10.1038\/s41583-020-0322-2","article-title":"Neuronal regulation of the blood-brain barrier and neurovascular coupling","volume":"21","author":"Kaplan","year":"2020","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"2741","DOI":"10.3389\/fphar.2021.754743","article-title":"The Contribution of Dysfunctional Chloride Channels to Neurovascular Deficiency and Neurodegeneration","volume":"12","author":"Gascoigne","year":"2021","journal-title":"Front. Pharmacol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1038\/sj.jcbfm.9600558","article-title":"Specific subtypes of cortical GABA interneurons contribute to the neurovascular coupling response to basal forebrain stimulation","volume":"28","author":"Kocharyan","year":"2008","journal-title":"J. Cereb. Blood Flow Metab."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"116034","DOI":"10.1016\/j.neuroimage.2019.116034","article-title":"Role of the inhibitory system in shaping the BOLD fMRI response","volume":"201","author":"Aksenov","year":"2019","journal-title":"Neuroimage"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1579","DOI":"10.1038\/jcbfm.2015.140","article-title":"Optogenetic stimulation of GABA neurons can decrease local neuronal activity while increasing cortical blood flow","volume":"35","author":"Anenberg","year":"2015","journal-title":"J. Cereb. Blood Flow Metab."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1157","DOI":"10.1152\/jn.00994.2014","article-title":"Interneurons contribute to the hemodynamic\/metabolic response to epileptiform discharges","volume":"115","author":"Saillet","year":"2016","journal-title":"J. Neurophysiol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1002\/(SICI)1096-9861(20000529)421:2<161::AID-CNE3>3.0.CO;2-F","article-title":"GABA neurons provide a rich input to microvessels but not nitric oxide neurons in the rat cerebral cortex: A means for direct regulation of local cerebral blood flow","volume":"421","author":"Vaucher","year":"2000","journal-title":"J. Comp. Neurol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"8940","DOI":"10.1523\/JNEUROSCI.3065-04.2004","article-title":"Cortical GABA interneurons in neurovascular coupling: Relays for subcortical vasoactive pathways","volume":"24","author":"Cauli","year":"2004","journal-title":"J. Neurosci."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"339","DOI":"10.1111\/j.1469-7610.2010.02307.x","article-title":"Annual Research Review: Development of the cerebral cortex: Implications for neurodevelopmental disorders","volume":"52","author":"Rubenstein","year":"2011","journal-title":"J. Child Psychol. Psychiatry"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"892784","DOI":"10.1155\/2012\/892784","article-title":"GABA through the ages: Regulation of cortical function and plasticity by inhibitory interneurons","volume":"2012","author":"Lehmann","year":"2012","journal-title":"Neural. Plast."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1669","DOI":"10.1038\/s41593-017-0020-1","article-title":"Thalamic functions in distributed cognitive control","volume":"20","author":"Halassa","year":"2017","journal-title":"Nat. Neurosci."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"13579","DOI":"10.1038\/ncomms13579","article-title":"Tectal-derived interneurons contribute to phasic and tonic inhibition in the visual thalamus","volume":"7","author":"Jager","year":"2016","journal-title":"Nat. Commun."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"130","DOI":"10.1126\/science.278.5335.130","article-title":"Functional dynamics of GABAergic inhibition in the thalamus","volume":"278","author":"Kim","year":"1997","journal-title":"Science"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1619","DOI":"10.1152\/physrev.00007.2017","article-title":"Hippocampal GABAergic Inhibitory Interneurons","volume":"97","author":"Pelkey","year":"2017","journal-title":"Physiol. Rev."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"146","DOI":"10.1016\/j.semcdb.2021.01.005","article-title":"GABAergic dysfunction, neural network hyperactivity and memory impairments in human aging and Alzheimer\u2019s disease","volume":"116","author":"Eich","year":"2021","journal-title":"Semin. Cell Dev. Biol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"140","DOI":"10.3389\/fncel.2017.00140","article-title":"Regulation of the Hippocampal Network by VGLUT3-Positive CCK- GABAergic Basket Cells","volume":"11","author":"Fasano","year":"2017","journal-title":"Front. Cell Neurosci."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"687","DOI":"10.1038\/nrn2207","article-title":"Long-term synaptic plasticity in hippocampal interneurons","volume":"8","author":"Kullmann","year":"2007","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"1311","DOI":"10.1038\/s41467-017-00956-z","article-title":"Hippocampal GABA enables inhibitory control over unwanted thoughts","volume":"8","author":"Schmitz","year":"2017","journal-title":"Nat. Commun."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"813749","DOI":"10.1155\/2011\/813749","article-title":"Interplay of amygdala and cingulate plasticity in emotional fear","volume":"2011","author":"Toyoda","year":"2011","journal-title":"Neural. Plast."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"1101","DOI":"10.1111\/j.1460-9568.2011.07609.x","article-title":"A new chapter in the field of memory: Adult hippocampal neurogenesis","volume":"33","author":"Koehl","year":"2011","journal-title":"Eur. J. Neurosci."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1080\/14734220510008012","article-title":"Formation of GABAergic synapses in the cerebellum","volume":"4","author":"Takayama","year":"2005","journal-title":"Cerebellum"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"527","DOI":"10.1002\/cne.902900407","article-title":"On the number of Purkinje cells in the human cerebellum: Unbiased estimates obtained by using the \u201cfractionator\u201d","volume":"290","author":"Nairn","year":"1989","journal-title":"J. Comp. Neurol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"367","DOI":"10.1016\/S0166-2236(98)01330-7","article-title":"The cerebellum: An overview","volume":"21","author":"Middleton","year":"1998","journal-title":"Trends. Neurosci."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"944","DOI":"10.1093\/schbul\/sbn070","article-title":"GABA neurons and the mechanisms of network oscillations: Implications for understanding cortical dysfunction in schizophrenia","volume":"34","author":"Lewis","year":"2008","journal-title":"Schizophr. Bull."},{"key":"ref_61","first-page":"2096","article-title":"When two wrongs make a right: Synchronized neuronal bursting from combined electrical and inhibitory coupling","volume":"375","author":"Reimbayev","year":"2017","journal-title":"Philos. Trans. A Math. Phys. Eng. Sci."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1038\/378075a0","article-title":"Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons","volume":"378","author":"Cobb","year":"1995","journal-title":"Nature"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1038\/25665","article-title":"A critical window for cooperation and competition among developing retinotectal synapses","volume":"395","author":"Zhang","year":"1998","journal-title":"Nature"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"10464","DOI":"10.1523\/JNEUROSCI.18-24-10464.1998","article-title":"Synaptic modifications in cultured hippocampal neurons: Dependence on spike timing, synaptic strength, and postsynaptic cell type","volume":"18","author":"Bi","year":"1998","journal-title":"J. Neurosci."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1111\/j.1469-7793.1998.237bu.x","article-title":"Long-term synaptic plasticity between pairs of individual CA3 pyramidal cells in rat hippocampal slice cultures","volume":"507","author":"Debanne","year":"1998","journal-title":"J. Physiol."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"150","DOI":"10.1016\/j.conb.2010.02.006","article-title":"Synchronous neural activity and memory formation","volume":"20","author":"Jutras","year":"2010","journal-title":"Curr. Opin. Neurobiol."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1016\/0091-3057(90)90052-J","article-title":"Modulation by estrogen and progesterone of the effect of muscimol on nociception in the spinal cord","volume":"37","author":"McCarthy","year":"1990","journal-title":"Pharmacol. Biochem. Behav."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"525","DOI":"10.1016\/0024-3205(77)90092-3","article-title":"Effect of muscimol, a GABA-mimetic agent, on dopamine metabolism in the mouse brain","volume":"21","author":"Biggio","year":"1977","journal-title":"Life Sci."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"1005","DOI":"10.1037\/0735-7044.108.5.1005","article-title":"Effects of muscimol applied to the basolateral amygdala on acquisition and expression of contextual fear conditioning in rats","volume":"108","author":"Helmstetter","year":"1994","journal-title":"Behav. Neurosci."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"719","DOI":"10.1152\/jn.00859.2003","article-title":"GABA neurotransmission in the cerebellar interposed nuclei: Involvement in classically conditioned eyeblinks and neuronal activity","volume":"91","author":"Aksenov","year":"2004","journal-title":"J. Neurophysiol."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1034\/j.1601-183X.2003.00037.x","article-title":"Model of autism: Increased ratio of excitation\/inhibition in key neural systems","volume":"2","author":"Rubenstein","year":"2003","journal-title":"Genes Brain Behav."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"1248","DOI":"10.1038\/s41380-019-0426-0","article-title":"Excitation-inhibition balance as a framework for investigating mechanisms in neuropsychiatric disorders","volume":"24","author":"Sohal","year":"2019","journal-title":"Mol. Psychiatry"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"367","DOI":"10.1038\/nn.3947","article-title":"Molecular mechanisms of epilepsy","volume":"18","author":"Staley","year":"2015","journal-title":"Nat. Neurosci."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1016\/0006-8993(78)90447-X","article-title":"Excitatory and inhibitory actions of GABA and glycine on embryonic chick spinal neurons in culture","volume":"144","author":"Obata","year":"1978","journal-title":"Brain Res."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"303","DOI":"10.1113\/jphysiol.1989.sp017762","article-title":"Giant synaptic potentials in immature rat CA3 hippocampal neurones","volume":"416","author":"Cherubini","year":"1989","journal-title":"J. Physiol."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"243","DOI":"10.1016\/S0896-6273(00)80265-2","article-title":"Ca2+ oscillations mediated by the synergistic excitatory actions of GABA(A) and NMDA receptors in the neonatal hippocampus","volume":"18","author":"Leinekugel","year":"1997","journal-title":"Neuron"},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"2340","DOI":"10.1152\/jn.1998.80.5.2340","article-title":"Temporal patterns and depolarizing actions of spontaneous GABAA receptor activation in granule cells of the early postnatal dentate gyrus","volume":"80","author":"Hollrigel","year":"1998","journal-title":"J. Neurophysiol."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"6414","DOI":"10.1523\/JNEUROSCI.16-20-06414.1996","article-title":"Excitatory GABA responses in embryonic and neonatal cortical slices demonstrated by gramicidin perforated-patch recordings and calcium imaging","volume":"16","author":"Owens","year":"1996","journal-title":"J. Neurosci."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"428","DOI":"10.1152\/jn.2000.84.1.428","article-title":"An excitatory GABAergic plexus in developing neocortical layer 1","volume":"84","author":"Dammerman","year":"2000","journal-title":"J. Neurophysiol."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"425","DOI":"10.1152\/jn.2001.85.1.425","article-title":"GABA, not glutamate, a primary transmitter driving action potentials in developing hypothalamic neurons","volume":"85","author":"Gao","year":"2001","journal-title":"J. Neurophysiol."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"429","DOI":"10.1111\/j.1469-7793.2001.0429c.xd","article-title":"GABA-mediated Ca2+ signalling in developing rat cerebellar Purkinje neurones","volume":"536","author":"Eilers","year":"2001","journal-title":"J. Physiol."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"371","DOI":"10.1113\/jphysiol.1995.sp020973","article-title":"Depolarizing GABA-activated Cl- channels in embryonic rat spinal and olfactory bulb cells","volume":"488","author":"Serafini","year":"1995","journal-title":"J. Physiol."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"411","DOI":"10.1113\/jphysiol.1994.sp020142","article-title":"Mechanisms of GABA and glycine depolarization-induced calcium transients in rat dorsal horn neurons","volume":"476","author":"Reichling","year":"1994","journal-title":"J. Physiol."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"728","DOI":"10.1038\/nrn920","article-title":"Excitatory actions of gaba during development: The nature of the nurture","volume":"3","year":"2002","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"757","DOI":"10.1113\/jphysiol.2009.183574","article-title":"How GABA generates depolarization","volume":"588","author":"Spitzer","year":"2010","journal-title":"J. Physiol."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1016\/S0168-0102(98)00099-6","article-title":"Simultaneous optical imaging of intracellular Cl\u2212 in neurons in different layers of rat neocortical slices: Advantages and limitations","volume":"32","author":"Fukuda","year":"1998","journal-title":"Neurosci. Res."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"447","DOI":"10.1016\/S0896-6273(00)00056-8","article-title":"A genetically encoded ratiometric indicator for chloride: Capturing chloride transients in cultured hippocampal neurons","volume":"27","author":"Kuner","year":"2000","journal-title":"Neuron"},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"1520","DOI":"10.1002\/jnr.21607","article-title":"Early postnatal development of rat brain: In vivo diffusion tensor imaging","volume":"86","author":"Bockhorst","year":"2008","journal-title":"J. Neurosci. Res."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"913","DOI":"10.1177\/0192623313503518","article-title":"The development of myelin in the brain of the juvenile rat","volume":"42","author":"Downes","year":"2014","journal-title":"Toxicol. Pathol."},{"key":"ref_90","first-page":"1406","article-title":"Normal myelination of the pediatric brain imaged with fluid-attenuated inversion-recovery (FLAIR) MR imaging","volume":"20","author":"Murakami","year":"1999","journal-title":"AJNR Am. J. Neuroradiol."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1146\/annurev.neuro.051508.135600","article-title":"The glial nature of embryonic and adult neural stem cells","volume":"32","author":"Kriegstein","year":"2009","journal-title":"Annu. Rev. Neurosci."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"481","DOI":"10.1016\/S0047-6374(01)00356-6","article-title":"Glial fibrillary acidic protein immunoreactive astrocytes in developing rat hippocampus","volume":"123","author":"Catalani","year":"2002","journal-title":"Mech. Ageing Dev."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"675","DOI":"10.1093\/cercor\/bhn112","article-title":"Quantification of brain maturation and growth patterns in C57BL\/6J mice via computational neuroanatomy of diffusion tensor images","volume":"19","author":"Baloch","year":"2009","journal-title":"Cereb. Cortex"},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"757","DOI":"10.1136\/adc.48.10.757","article-title":"Quantitative growth and development of human brain","volume":"48","author":"Dobbing","year":"1973","journal-title":"Arch. Dis. Child."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1016\/0378-3782(79)90022-7","article-title":"Comparative aspects of the brain growth spurt","volume":"3","author":"Dobbing","year":"1979","journal-title":"Early Hum. Dev."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"340","DOI":"10.1002\/(SICI)1096-9861(19960923)373:3<340::AID-CNE3>3.0.CO;2-2","article-title":"Quantitative aspects of synaptogenesis in the rat barrel field cortex with special reference to GABA circuitry","volume":"373","author":"Micheva","year":"1996","journal-title":"J. Comp. Neurol."},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"1909","DOI":"10.1016\/S0024-3205(02)01492-3","article-title":"Development of the corpus callosum in childhood, adolescence and early adulthood","volume":"70","author":"Keshavan","year":"2002","journal-title":"Life Sci."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.pneurobio.2013.04.001","article-title":"Brain development in rodents and humans: Identifying benchmarks of maturation and vulnerability to injury across species","volume":"106","author":"Semple","year":"2013","journal-title":"Prog. Neurobiol."},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"841","DOI":"10.1097\/NEN.0b013e31822f471c","article-title":"Late development of the GABAergic system in the human cerebral cortex and white matter","volume":"70","author":"Xu","year":"2011","journal-title":"J. Neuropathol. Exp. Neurol."},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"10372","DOI":"10.1523\/JNEUROSCI.19-23-10372.1999","article-title":"The establishment of GABAergic and glutamatergic synapses on CA1 pyramidal neurons is sequential and correlates with the development of the apical dendrite","volume":"19","author":"Tyzio","year":"1999","journal-title":"J. Neurosci."},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"9770","DOI":"10.1523\/JNEUROSCI.21-24-09770.2001","article-title":"Early development of neuronal activity in the primate hippocampus in utero","volume":"21","author":"Khazipov","year":"2001","journal-title":"J. Neurosci."},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"1937","DOI":"10.1046\/j.0953-816x.2001.01823.x","article-title":"Activity- and age-dependent GABAergic synaptic plasticity in the developing rat hippocampus","volume":"14","author":"Gubellini","year":"2001","journal-title":"Eur. J. Neurosci."},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"613","DOI":"10.1177\/1073858411422114","article-title":"Development of the GABAergic system from birth to adolescence","volume":"18","author":"Kilb","year":"2012","journal-title":"Neuroscientist"},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"583477","DOI":"10.3389\/fnins.2020.583477","article-title":"Sex Differences in the Development of the Rodent Corticolimbic System","volume":"14","author":"Premachandran","year":"2020","journal-title":"Front. Neurosci."},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"1982","DOI":"10.1111\/ejn.12606","article-title":"Functions of gamma-band synchronization in cognition: From single circuits to functional diversity across cortical and subcortical systems","volume":"39","author":"Bosman","year":"2014","journal-title":"Eur. J. Neurosci."},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"2049","DOI":"10.1126\/science.1071111","article-title":"Correlated bursts of activity in the neonatal hippocampus in vivo","volume":"296","author":"Leinekugel","year":"2002","journal-title":"Science"},{"key":"ref_107","doi-asserted-by":"crossref","first-page":"12956","DOI":"10.1523\/JNEUROSCI.2890-08.2008","article-title":"Postnatal differentiation of basket cells from slow to fast signaling devices","volume":"28","author":"Doischer","year":"2008","journal-title":"J. Neurosci."},{"key":"ref_108","doi-asserted-by":"crossref","first-page":"7040","DOI":"10.1523\/JNEUROSCI.0105-09.2009","article-title":"Transcriptional and electrophysiological maturation of neocortical fast-spiking GABAergic interneurons","volume":"29","author":"Okaty","year":"2009","journal-title":"J. Neurosci."},{"key":"ref_109","doi-asserted-by":"crossref","first-page":"849","DOI":"10.1111\/j.1460-9568.2008.06401.x","article-title":"Developmental profile of GABAA-mediated synaptic transmission in pyramidal cells of the somatosensory cortex","volume":"28","author":"Kobayashi","year":"2008","journal-title":"Eur. J. Neurosci."},{"key":"ref_110","first-page":"463","article-title":"Epigenetic modulation during hippocampal development","volume":"9","author":"Fan","year":"2018","journal-title":"Biomed. Rep."},{"key":"ref_111","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1046\/j.1460-9568.2002.02073.x","article-title":"Early sequential formation of functional GABA(A) and glutamatergic synapses on CA1 interneurons of the rat foetal hippocampus","volume":"16","author":"Hennou","year":"2002","journal-title":"Eur. J. Neurosci."},{"key":"ref_112","doi-asserted-by":"crossref","first-page":"422","DOI":"10.1016\/j.tins.2004.05.002","article-title":"Interneurons set the tune of developing networks","volume":"27","author":"Khalilov","year":"2004","journal-title":"Trends Neurosci."},{"key":"ref_113","doi-asserted-by":"crossref","first-page":"13832","DOI":"10.1038\/s41598-020-70818-0","article-title":"Effects of neonatal isoflurane anesthesia exposure on learning-specific and sensory systems in adults","volume":"10","author":"Aksenov","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_114","doi-asserted-by":"crossref","first-page":"645","DOI":"10.1038\/nature00779","article-title":"Origin of GABAergic neurons in the human neocortex","volume":"417","author":"Letinic","year":"2002","journal-title":"Nature"},{"key":"ref_115","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1186\/2045-3701-3-19","article-title":"Development and specification of GABAergic cortical interneurons","volume":"3","author":"Kelsom","year":"2013","journal-title":"Cell Biosci."},{"key":"ref_116","doi-asserted-by":"crossref","first-page":"253","DOI":"10.1002\/cne.902410302","article-title":"Cytoarchitectonic development of the prefrontal cortex in the rat","volume":"241","author":"Uylings","year":"1985","journal-title":"J. Comp. Neurol."},{"key":"ref_117","doi-asserted-by":"crossref","first-page":"4556","DOI":"10.1111\/bph.12643","article-title":"Developmental rodent models of fear and anxiety: From neurobiology to pharmacology","volume":"171","author":"Ganella","year":"2014","journal-title":"Br. J. Pharmacol."},{"key":"ref_118","first-page":"449","article-title":"Maturation of the adolescent brain","volume":"9","author":"Arain","year":"2013","journal-title":"Neuropsychiatr. Dis. Treat."},{"key":"ref_119","doi-asserted-by":"crossref","first-page":"10","DOI":"10.7554\/eLife.59272","article-title":"Dual midbrain and forebrain origins of thalamic inhibitory interneurons","volume":"10","author":"Jager","year":"2021","journal-title":"eLife"},{"key":"ref_120","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1016\/0378-3782(91)90033-Y","article-title":"Early development of the human thalamus: Golgi and Nissl study","volume":"27","author":"Mojsilovic","year":"1991","journal-title":"Early Hum. Dev."},{"key":"ref_121","doi-asserted-by":"crossref","first-page":"e345","DOI":"10.1002\/wdev.345","article-title":"Development of the thalamus: From early patterning to regulation of cortical functions","volume":"8","author":"Nakagawa","year":"2019","journal-title":"Wiley Interdiscip. Rev. Dev. Biol."},{"key":"ref_122","doi-asserted-by":"crossref","first-page":"9067","DOI":"10.1523\/JNEUROSCI.0796-14.2014","article-title":"Development of thalamocortical connectivity during infancy and its cognitive correlations","volume":"34","author":"Alcauter","year":"2014","journal-title":"J. Neurosci."},{"key":"ref_123","doi-asserted-by":"crossref","first-page":"7246","DOI":"10.1523\/JNEUROSCI.0607-16.2016","article-title":"Lack of Intrinsic GABAergic Connections in the Thalamic Reticular Nucleus of the Mouse","volume":"36","author":"Hou","year":"2016","journal-title":"J. Neurosci."},{"key":"ref_124","doi-asserted-by":"crossref","first-page":"7079","DOI":"10.1523\/JNEUROSCI.0957-09.2009","article-title":"Laminar fate and phenotype specification of cerebellar GABAergic interneurons","volume":"29","author":"Leto","year":"2009","journal-title":"J. Neurosci."},{"key":"ref_125","doi-asserted-by":"crossref","first-page":"154","DOI":"10.1016\/j.pedneo.2017.08.007","article-title":"Effect of multiple neonatal sevoflurane exposures on hippocampal apolipoprotein E levels and learning and memory abilities","volume":"59","author":"Jiang","year":"2018","journal-title":"Pediatr. Neonatol."},{"key":"ref_126","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1016\/j.neuroscience.2010.10.009","article-title":"The glutaminergic, GABAergic, dopaminergic but not cholinergic neurons are susceptible to anaesthesia-induced cell death in the rat developing brain","volume":"174","author":"Zhou","year":"2011","journal-title":"Neuroscience"},{"key":"ref_127","doi-asserted-by":"crossref","first-page":"443","DOI":"10.1093\/bja\/aet469","article-title":"Brain regional vulnerability to anaesthesia-induced neuroapoptosis shifts with age at exposure and extends into adulthood for some regions","volume":"113","author":"Deng","year":"2014","journal-title":"Br. J. Anaesth."},{"key":"ref_128","doi-asserted-by":"crossref","first-page":"373","DOI":"10.3389\/fncel.2017.00373","article-title":"Propofol Exposure in Early Life Induced Developmental Impairments in the Mouse Cerebellum","volume":"11","author":"Xiao","year":"2017","journal-title":"Front. Cell Neurosci."},{"key":"ref_129","doi-asserted-by":"crossref","first-page":"472","DOI":"10.1016\/j.nbd.2019.01.016","article-title":"Neonatal general anesthesia causes lasting alterations in excitatory and inhibitory synaptic transmission in the ventrobasal thalamus of adolescent female rats","volume":"127","author":"Woodward","year":"2019","journal-title":"Neurobiol. Dis."},{"key":"ref_130","doi-asserted-by":"crossref","first-page":"624","DOI":"10.1097\/ALN.0000000000000981","article-title":"Epigenetic Manipulation of Brain-derived Neurotrophic Factor Improves Memory Deficiency Induced by Neonatal Anesthesia in Rats","volume":"124","author":"Wu","year":"2016","journal-title":"Anesthesiology"},{"key":"ref_131","doi-asserted-by":"crossref","first-page":"243","DOI":"10.1097\/ALN.0b013e31817f5c47","article-title":"Inhalational anesthetics induce cell damage by disruption of intracellular calcium homeostasis with different potencies","volume":"109","author":"Yang","year":"2008","journal-title":"Anesthesiology"},{"key":"ref_132","doi-asserted-by":"crossref","first-page":"258","DOI":"10.1007\/s12975-012-0233-2","article-title":"Bench to Cribside: The Path for Developing a Neuroprotectant","volume":"4","author":"Ramanantsoa","year":"2013","journal-title":"Transl. Stroke Res."},{"key":"ref_133","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1007\/s12975-013-0314-x","article-title":"Ionic regulation of cell volume changes and cell death after ischemic stroke","volume":"5","author":"Song","year":"2014","journal-title":"Transl. Stroke Res."},{"key":"ref_134","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1186\/1423-0127-17-14","article-title":"Region-specific effects on brain metabolites of hypoxia and hyperoxia overlaid on cerebral ischemia in young and old rats: A quantitative proton magnetic resonance spectroscopy study","volume":"17","author":"Macri","year":"2010","journal-title":"J. Biomed. Sci."},{"key":"ref_135","doi-asserted-by":"crossref","first-page":"e1311","DOI":"10.1038\/cddis.2014.275","article-title":"Ketamine alters cortical integration of GABAergic interneurons and induces long-term sex-dependent impairments in transgenic Gad67-GFP mice","volume":"5","author":"Aligny","year":"2014","journal-title":"Cell Death Dis."},{"key":"ref_136","doi-asserted-by":"crossref","first-page":"288","DOI":"10.1097\/ALN.0000000000001470","article-title":"Sevoflurane Exposure during the Critical Period Affects Synaptic Transmission and Mitochondrial Respiration but Not Long-term Behavior in Mice","volume":"126","author":"Chung","year":"2017","journal-title":"Anesthesiology"},{"key":"ref_137","doi-asserted-by":"crossref","first-page":"e81","DOI":"10.1016\/j.bja.2019.12.032","article-title":"Sex differences in neurodevelopmental abnormalities caused by early-life anaesthesia exposure: A narrative review","volume":"124","author":"Cabrera","year":"2020","journal-title":"Br. J. Anaesth."},{"key":"ref_138","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1016\/j.physbeh.2016.08.030","article-title":"Eyeblink classical conditioning and BOLD fMRI of anesthesia-induced changes in the developing brain","volume":"167","author":"Aksenov","year":"2016","journal-title":"Physiol. Behav."},{"key":"ref_139","doi-asserted-by":"crossref","first-page":"571486","DOI":"10.3389\/fnins.2020.571486","article-title":"Behavior and regional cortical BOLD signal fluctuations are altered in adult rabbits after neonatal volatile anesthetic exposure","volume":"14","author":"Drobyshevsky","year":"2020","journal-title":"Front. Neurosci."},{"key":"ref_140","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1007\/s10827-019-00736-2","article-title":"Oscillations and concentration dynamics of brain tissue oxygen in neonates and adults","volume":"48","author":"Doubovikov","year":"2020","journal-title":"J. Comput. Neurosci."},{"key":"ref_141","doi-asserted-by":"crossref","first-page":"311","DOI":"10.1007\/978-1-4939-3023-4_39","article-title":"Spontaneous Fluctuations of PO2 in the Rabbit Somatosensory Cortex","volume":"876","author":"Linsenmeier","year":"2016","journal-title":"Adv. Exp. Med. Biol."},{"key":"ref_142","doi-asserted-by":"crossref","first-page":"2189","DOI":"10.1161\/01.STR.0000136149.81831.c5","article-title":"Apoptotic and necrotic death mechanisms are concomitantly activated in the same cell after cerebral ischemia","volume":"35","author":"Can","year":"2004","journal-title":"Stroke"},{"key":"ref_143","doi-asserted-by":"crossref","first-page":"1889","DOI":"10.1089\/ars.2010.3474","article-title":"Significance of Brain Tissue Oxygenation and the Arachidonic Acid Cascade in Stroke","volume":"14","author":"Rink","year":"2011","journal-title":"Antioxidants Redox Signal."},{"key":"ref_144","doi-asserted-by":"crossref","first-page":"101744","DOI":"10.1016\/j.jchemneu.2020.101744","article-title":"Effects of chronic hypoxia on the expression of seladin-1\/Tuj1 and the number of dark neurons of hippocampus","volume":"104","author":"Mahakizadeh","year":"2020","journal-title":"J. Chem. Neuroanat."},{"key":"ref_145","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1016\/j.neuroscience.2018.04.026","article-title":"Temporal and Spatial Changes in Glial Cells During Chronic Hypobaric Hypoxia: Role in Neurodegeneration","volume":"383","author":"Dheer","year":"2018","journal-title":"Neuroscience"},{"key":"ref_146","doi-asserted-by":"crossref","first-page":"2977","DOI":"10.1016\/j.bbamcr.2016.09.012","article-title":"Activation of apoptosis signalling pathways by reactive oxygen species","volume":"1863","year":"2016","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_147","doi-asserted-by":"crossref","first-page":"132","DOI":"10.3389\/fcell.2018.00132","article-title":"Reactive Oxygen Species Formation in the Brain at Different Oxygen Levels: The Role of Hypoxia Inducible Factors","volume":"6","author":"Chen","year":"2018","journal-title":"Front. Cell Dev. Biol."},{"key":"ref_148","doi-asserted-by":"crossref","first-page":"545","DOI":"10.1196\/annals.1333.062","article-title":"Oxidative stress and neurodegeneration","volume":"1043","author":"Moreira","year":"2005","journal-title":"Ann. N. Y. Acad. Sci."},{"key":"ref_149","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1016\/S0928-4680(00)00053-5","article-title":"Oxidative stress and apoptosis","volume":"7","author":"Kannan","year":"2000","journal-title":"Pathophysiology"},{"key":"ref_150","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1016\/j.ceca.2004.02.013","article-title":"Calcium and pH homeostasis in neurons during hypoxia and ischemia","volume":"36","author":"Yao","year":"2004","journal-title":"Cell Calcium"},{"key":"ref_151","doi-asserted-by":"crossref","first-page":"R9","DOI":"10.1152\/ajpregu.2000.279.1.R9","article-title":"Critical oxygen tension in rat brain: A combined (31)P-NMR and EPR oximetry study","volume":"279","author":"Rolett","year":"2000","journal-title":"Am. J. Physiol. Regul. Integr. Comp. Physiol."},{"key":"ref_152","doi-asserted-by":"crossref","first-page":"54","DOI":"10.1203\/00006450-199007000-00013","article-title":"Cerebral energy metabolism and oxygen state during hypoxia in neonate and adult dogs","volume":"28","author":"Nioka","year":"1990","journal-title":"Pediatr. Res."},{"key":"ref_153","doi-asserted-by":"crossref","first-page":"469","DOI":"10.1016\/j.nbd.2013.10.025","article-title":"Nicotinamide pre-treatment ameliorates NAD(H) hyperoxidation and improves neuronal function after severe hypoxia","volume":"62","author":"Shetty","year":"2014","journal-title":"Neurobiol. Dis."},{"key":"ref_154","doi-asserted-by":"crossref","first-page":"510","DOI":"10.1097\/ALN.0000000000000278","article-title":"Sevoflurane induces tau phosphorylation and glycogen synthase kinase 3\u03b2 activation in young mice","volume":"121","author":"Tao","year":"2014","journal-title":"Anesthesiology"},{"key":"ref_155","doi-asserted-by":"crossref","first-page":"3","DOI":"10.3892\/mmr.2015.3424","article-title":"Effect of the inhaled anesthetics isoflurane, sevoflurane and desflurane on the neuropathogenesis of Alzheimer\u2019s disease (Review)","volume":"12","author":"Jiang","year":"2015","journal-title":"Mol. Med. Rep."},{"key":"ref_156","doi-asserted-by":"crossref","first-page":"620","DOI":"10.1001\/archneurol.2009.48","article-title":"The Common Inhalational Anesthetic Sevoflurane Induces Apoptosis and Increases \u03b2-Amyloid Protein Levels","volume":"66","author":"Dong","year":"2009","journal-title":"Arch. Neurol."},{"key":"ref_157","doi-asserted-by":"crossref","first-page":"1385","DOI":"10.1016\/S0022-5223(03)00711-6","article-title":"Neurodevelopmental status at eight years in children with dextro-transposition of the great arteries: The Boston Circulatory Arrest Trial","volume":"126","author":"Bellinger","year":"2003","journal-title":"J. Thorac. Cardiovasc. Surg."},{"key":"ref_158","doi-asserted-by":"crossref","first-page":"3127","DOI":"10.1007\/s10803-019-04034-9","article-title":"Exposure to General Anesthesia May Contribute to the Association between Cesarean Delivery and Autism Spectrum Disorder","volume":"49","author":"Meiri","year":"2019","journal-title":"J. Autism Dev. Disord."},{"key":"ref_159","first-page":"73","article-title":"Previous Exposure to Anesthesia and Autism Spectrum Disorder (ASD): A Puerto Rican Population-Based Sibling Cohort Study","volume":"108","author":"Creagh","year":"2016","journal-title":"Bol. Asoc. Med. Puerto Rico"},{"key":"ref_160","doi-asserted-by":"crossref","first-page":"37","DOI":"10.3389\/fncir.2018.00037","article-title":"PV Interneurons: Critical Regulators of E\/I Balance for Prefrontal Cortex-Dependent Behavior and Psychiatric Disorders","volume":"12","author":"Ferguson","year":"2018","journal-title":"Front. Neural Circuits"},{"key":"ref_161","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1152\/jn.00586.2004","article-title":"Glutamate neurotransmission in the cerebellar interposed nuclei: Involvement in classically conditioned eyeblinks and neuronal activity","volume":"93","author":"Aksenov","year":"2005","journal-title":"J. Neurophysiol."},{"key":"ref_162","doi-asserted-by":"crossref","first-page":"1141","DOI":"10.1016\/j.bja.2021.01.017","article-title":"Behavioural impairments after exposure of neonatal mice to propofol are accompanied by reductions in neuronal activity in cortical circuitry","volume":"126","author":"Zhou","year":"2021","journal-title":"Br. J. Anaesth."},{"key":"ref_163","first-page":"527","article-title":"In vivo magnetic resonance spectroscopy: Basic methodology and clinical applications","volume":"39","year":"2009","journal-title":"Eur. Biophys. J."},{"key":"ref_164","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1016\/j.pnmrs.2011.06.001","article-title":"In vivo magnetic resonance spectroscopy of GABA: A methodological review","volume":"60","author":"Puts","year":"2012","journal-title":"Prog. Nucl. Magn. Reson. Spectrosc."},{"key":"ref_165","doi-asserted-by":"crossref","first-page":"5662","DOI":"10.1073\/pnas.90.12.5662","article-title":"Localized 1H NMR measurements of gamma-aminobutyric acid in human brain in vivo","volume":"90","author":"Rothman","year":"1993","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_166","doi-asserted-by":"crossref","first-page":"1276","DOI":"10.1002\/mrm.21383","article-title":"Spatial effects in the detection of gamma-aminobutyric acid: Improved sensitivity at high fields using inner volume saturation","volume":"58","author":"Edden","year":"2007","journal-title":"Magn. Reason. Med."},{"key":"ref_167","doi-asserted-by":"crossref","first-page":"1009","DOI":"10.1002\/mrm.10146","article-title":"Direct in vivo measurement of human cerebral GABA concentration using MEGA-editing at 7 Tesla","volume":"47","author":"Terpstra","year":"2002","journal-title":"Magn. Reason. Med."},{"key":"ref_168","doi-asserted-by":"crossref","first-page":"096601","DOI":"10.1088\/0034-4885\/76\/9\/096601","article-title":"The physics of functional magnetic resonance imaging (fMRI)","volume":"76","author":"Buxton","year":"2013","journal-title":"Rep. Prog. Phys."},{"key":"ref_169","doi-asserted-by":"crossref","first-page":"2722","DOI":"10.1111\/ejn.13384","article-title":"Blood oxygenation level dependent signal and neuronal adaptation to optogenetic and sensory stimulation in somatosensory cortex in awake animals","volume":"44","author":"Aksenov","year":"2016","journal-title":"Eur. J. Neurosci."},{"key":"ref_170","doi-asserted-by":"crossref","first-page":"593","DOI":"10.1016\/j.conb.2007.11.002","article-title":"MRI contrast agents for functional molecular imaging of brain activity","volume":"17","author":"Jasanoff","year":"2007","journal-title":"Curr. Opin. Neurobiol."},{"key":"ref_171","doi-asserted-by":"crossref","first-page":"1458","DOI":"10.1152\/jn.00362.2020","article-title":"The intrinsic neonatal hippocampal network: RsfMRI findings","volume":"124","author":"Howell","year":"2020","journal-title":"J. Neurophysiol."},{"key":"ref_172","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1016\/j.siny.2006.07.006","article-title":"Diffusion tensor imaging of brain development","volume":"11","author":"Dubois","year":"2006","journal-title":"Semin. Fetal Neonatal Med."},{"key":"ref_173","doi-asserted-by":"crossref","first-page":"316","DOI":"10.1016\/j.nurt.2007.05.011","article-title":"Diffusion tensor imaging of the brain","volume":"4","author":"Alexander","year":"2007","journal-title":"Neurotherapeutics"},{"key":"ref_174","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1148\/radiographics.15.1.7899611","article-title":"Helical CT: Practical considerations and potential pitfalls","volume":"15","author":"Silverman","year":"1995","journal-title":"Radiographics"},{"key":"ref_175","doi-asserted-by":"crossref","first-page":"1112","DOI":"10.1016\/j.neuron.2013.10.017","article-title":"EEG and MEG: Relevance to neuroscience","volume":"80","year":"2013","journal-title":"Neuron"},{"key":"ref_176","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1016\/j.ymeth.2006.12.008","article-title":"Cognitive neuroscience of creativity: EEG based approaches","volume":"42","author":"Srinivasan","year":"2007","journal-title":"Methods"},{"key":"ref_177","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1016\/j.neuron.2019.07.001","article-title":"Magnetoencephalography in Cognitive Neuroscience: A Primer","volume":"104","author":"Gross","year":"2019","journal-title":"Neuron"},{"key":"ref_178","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1113\/expphysiol.2004.029512","article-title":"Laser Doppler flowmetry is valid for measurement of cerebral blood flow autoregulation lower limit in rats","volume":"90","author":"Tonnesen","year":"2005","journal-title":"Exp. Physiol."},{"key":"ref_179","doi-asserted-by":"crossref","first-page":"8108","DOI":"10.1038\/s41598-018-26326-3","article-title":"Three dimensional two-photon brain imaging in freely moving mice using a miniature fiber coupled microscope with active axial-scanning","volume":"8","author":"Ozbay","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_180","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1093\/cercor\/13.1.25","article-title":"Fast-spike interneurons and feedforward inhibition in awake sensory neocortex","volume":"13","author":"Swadlow","year":"2003","journal-title":"Cereb. Cortex"},{"key":"ref_181","doi-asserted-by":"crossref","first-page":"1521","DOI":"10.1007\/s00221-019-05528-9","article-title":"The effect of sevoflurane and isoflurane anesthesia on single unit and local field potentials","volume":"237","author":"Aksenov","year":"2019","journal-title":"Exp. Brain Res."},{"key":"ref_182","doi-asserted-by":"crossref","first-page":"815","DOI":"10.1016\/j.neuroscience.2005.03.064","article-title":"Anesthesia induces neuronal cell death in the developing rat brain via the intrinsic and extrinsic apoptotic pathways","volume":"135","author":"Yon","year":"2005","journal-title":"Neuroscience"},{"key":"ref_183","doi-asserted-by":"crossref","first-page":"286","DOI":"10.1097\/ANA.0b013e3181a71f11","article-title":"A retrospective cohort study of the association of anesthesia and hernia repair surgery with behavioral and developmental disorders in young children","volume":"21","author":"Sun","year":"2009","journal-title":"J. Neurosurg. Anesthesiol."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/22\/23\/12951\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T07:37:46Z","timestamp":1760168266000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/22\/23\/12951"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,11,30]]},"references-count":183,"journal-issue":{"issue":"23","published-online":{"date-parts":[[2021,12]]}},"alternative-id":["ijms222312951"],"URL":"https:\/\/doi.org\/10.3390\/ijms222312951","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,11,30]]}}}